Preferential Begging Responses of Shiny Cowbirds to the Conspecific Chatter Call

Avian brood parasites lay their eggs into the nests of other species, which incubate them and raise the chicks until their independence. Despite living their early weeks of life surrounded by heterospecifics, young brood parasites have the ability to recognize and associate to conspecifics after independence. It has been proposed that the initial conspecific recognition develops when a young parasite encounters a unique species-specific signal that triggers the learning of other aspects of the producer of the signal. For cowbirds (Molothrus spp.), this species-specific signal is hypothesized to be the chatter call. Young birds also could express auditory biases, which in some cases lead to discrimination in favor of conspecific songs. Therefore, the perceptual selectivity for chatters might be also present in nestlings. Our aim was to assess if nestlings of the shiny cowbird (M. bonariensis) present a preferential begging response to conspecific chatter calls. We evaluated if they respond more to the parasitic vocalization than host chicks and if they respond more to the chatter than to heterospecific nonhost calls. We tested shiny cowbird chicks reared by chalk-browed mockingbirds (Mimus saturninus) or house wrens (Troglodytes aedon) and host chicks, as control species. We randomly presented to 6-day-old chicks the following playback treatments: (1) conspecific chatter calls, (2) host calls, used as positive controls, and (3) nonhost calls, used as negative control. We measured if chicks begged during the playback treatments and the begging intensity. When responding to the playback of chatter calls, shiny cowbird chicks begged at a higher frequency and more intensively than host chicks. Shiny cowbird chicks reared by mockingbirds begged more intensively to playbacks of conspecific chatter calls than to host calls, while those reared by wrens begged with a similar intensity to playbacks of conspecific chatter and host calls. On the contrary, wren nestlings begged more intensively to playbacks of the wren call than to chatter calls. Mockingbird nestlings did not beg during any treatment. None of the three species begged during the playback of nonhost calls. Our results show that the chatter call produced a preferential begging response in cowbird nestlings, which may be the beginning of a process of conspecific recognition.

Parasite egg recognition based on multicomponent cues by green-backed tits (Parus monticolus)

Egg recognition and rejection is a common and effective anti-parasitism adaptation in bird hosts. Hosts reject alien eggs using recognition signals such as egg ground color and maculation. Green-backed tits ( Parus monticolus) have a highly developed capability for recognizing parasite eggs, but the cues used for egg recognition are unclear. We combined avian visual perceptual modeling and field experiments to explore the effects of egg ground color and maculation on the recognition of parasite eggs. P. monticolus uses a multi-cue with possible hierarchical mechanism for egg recognition. The mechanism of egg recognition in P. monticolus appears to be a specific adaptation to the phenotypes of eggs laid by local brood parasites.

Tricking Parents: A Review of Mechanisms and Signals of Host Manipulation by Brood-Parasitic Young

Obligate avian brood parasites depend entirely on heterospecific hosts for rearing their offspring. From hatching until independence, the young parasites must deal with the challenge of obtaining sufficient parental care from foster parents that are attuned to provisioning their own offspring. Parent-offspring communication is mediated by complex begging displays in which nestlings and fledglings exhibit visual (e.g., gaping and postures) and vocal (e.g., begging calls) traits that serve as signals to parents to adjust and allocate parental effort. Parasites can manipulate host parental behavior by exploiting these stable parent-offspring communication systems in their favor. During the past 30 years, the study of host exploitation by parasitic chicks has yielded important insights into the function and evolution of manipulative signals in brood parasites. However, despite these major advances, there are still important gaps in our knowledge about how parasitic nestling and fledglings tune into the host’s communication channels and the adaptive value of the visual and acoustic signals they exhibit. Here we review the literature pertaining to host manipulation by parasitic young, focusing on four non-mutually exclusive mechanisms (i.e., host chick mimicry, begging exaggeration, host-attuned begging calls, and sensory exploitation) and the function and evolution of the signals involved, with the aim to summarize and discuss putative adaptations for stimulating parental feeding and escaping host discrimination. Finally, we bring some concluding remarks and suggest directions for future research on the ways in which brood parasites adapt to the communication systems of other birds to exploit the necessary parental care.

Decoupled Acoustic and Visual Components in the Multimodal Signals of the Common Cuckoo (Cuculus canorus)

Because of its parasitic habits, reproduction costs of the common cuckoo (Cuculus canorus) are mostly spent in pre-laying activities. Female costs are limited to searching host nests and laying eggs, whereas, males spend time in performing intense vocal displays, possibly with territorial purpose. This last aspect, together with a sexual plumage dimorphism, points to both intra- and inter-sexual selections operating within this species. One element triggering sexual selection is a differential fitness accrued by different phenotypes. Before analyzing possible sexual selection mechanisms operating in cuckoos, it is therefore necessary to verify whether there is a variability among male secondary characters by describing and quantifying them. Here we aimed to quantitatively characterize the main two potential candidates of sexual selection traits, i.e., calls and displays, shown by males at perches. During the 2019 breeding season, in a site within the Po Plain, we both audio and video recorded cuckoo males at five different perches. We analyzed acoustic variables as well as display sequences searching for potential correlations. We found a significant variation among calls that could be clustered into four vocal types. We also found that no visual displays were associated with vocal displays; cuckoo males were either vocal and motionless or soundless and active. We discuss our results under the perspective of the potential value of sexual selection in brood parasites and its role in its parasitic habit.

The Evolution of Predator Resemblance in Avian Brood Parasites

Predators have profound effects on prey behavior and some adult brood parasites use predator resemblance to exploit the antipredator defenses of their hosts. Clarifying host perception of such stimuli is important for understanding the adaptive significance of adult brood parasite characteristics, and the mechanisms by which they misdirect hosts. Here I review the literature to explore the adaptive basis of predator resemblance in avian brood parasites, and natural variation in host responses to these stimuli. I also provide a framework for the information ecology of predator resemblance, which is based on the principles of signal detection theory and draws from empirical evidence from the common cuckoo, Cuculus canorus, as the most widely studied system. In this species, visual and acoustic hawk-like stimuli are effective in manipulating host defenses. Overall, contrasts across host responses suggest that different modalities of information can have independent effects on hosts, and that predator resemblance takes advantage of multiple sensory and cognitive processes. Host perception of these stimuli and the degree to which they are processed in an integrated manner, and the physiological processes underlying regulation of the responses, present new avenues for brood parasitism research.

The Perceptual and Cognitive Processes That Govern Egg Rejection in Hosts of Avian Brood Parasites

Hosts of avian brood parasites are under intense selective pressure to prevent or reduce the cost of parasitism. Many have evolved refined egg discrimination abilities, which can select for eggshell mimicry in their parasite. A classic assumption underlying these coevolutionary dynamics is that host egg recognition depends on the perceivable difference between their own eggs and those of their parasite. Over the past two decades, the receptor noise-limited (RNL) model has contributed to our understanding of these coevolutionary interactions by providing researchers a method to predict a host’s ability to discriminate a parasite’s egg from its own. Recent research has shown that some hosts are more likely to reject brown eggs than blue eggs, regardless of the perceived differences to their own. Such responses suggest that host egg recognition may be due to perceptual or cognitive processes not currently predictable by the RNL model. In this perspective, we discuss the potential value of using the RNL model as a null model to explore alternative perceptual processes and higher-order cognitive processes that could explain how and why some hosts make seemingly counter-intuitive decisions. Further, we outline experiments that should be fruitful for determining the perceptual and cognitive processing used by hosts for egg recognition tasks.

Host eyes, brains and their brood parasites

1. Brood parasites interact with their hosts for exploitation of host parental abilities and the associated resources. This results in coevolutionary interactions of hosts and parasites. 2. A prime example of such a common specialist brood parasite is the common cuckoo Cuculus canorus and its host races. Hosts use their cognitive abilities to identify parasites and vice versa for their ability to discriminate among potential hosts. 3. We predicted that parasites with relatively large brains for their body size should be more successful at avoiding their hosts, and that hosts with small brains for their body size should more often be exploited by parasites. We also predicted that hosts with relatively large eyes for their body size would have superior discriminatory abilities allowing for superior discrimination against brood parasites. Finally, we predicted that visual ability of specific cuckoo hosts would have evolved exaggerated visual ability as estimated from the relative size of their optic tectum would have resulted in such hosts being more successful as reflected by their higher rate of parasitism. 4. Interspecific variation in size of brain, eye, optic tectum, telencephalon and cerebellum were consistent with these predictions.

Embryo movement is more frequent in avian brood parasites than birds with parental reproductive strategies

Movement of the embryo is essential for musculoskeletal development in vertebrates, yet little is known about whether, and why, species vary. Avian brood parasites exhibit feats of strength in early life as adaptations to exploit the hosts that rear them. We hypothesized that an increase in embryonic movement could allow brood parasites to develop the required musculature for these demands. We measured embryo movement across incubation for multiple brood-parasitic and non-parasitic bird species. Using a phylogenetically controlled analysis, we found that brood parasites exhibited significantly increased muscular movement during incubation compared to non-parasites. This suggests that increased embryo movement may facilitate the development of the stronger musculoskeletal system required for the demanding tasks undertaken by young brood parasites.

Variation in the Non-mimetic Vocalizations of Brood-Parasitic Indigobirds and Their Potential Role in Speciation

Indigobirds (Vidua spp.) are obligate brood parasites in which imprinting on heterospecific hosts shapes adult vocal behavior and mating preferences. Adult male indigobirds mimic the songs and other vocalizations of their respective hosts, which signals their own host environment to prospective mates and has important implications for speciation. In this study, we examined variation within and among indigobird species in the non-mimetic components of their vocal behavior, including both chatter calls and their impressive repertoires of intricate non-mimicry songs. We test whether indigobird species in Tanzania (V. chalybeata, V. codringtoni, V. funerea, and V. purpurascens) differ consistently in general features of their non-mimetic vocalizations, and we test whether local ecological conditions influence vocal behavior. Indigobird non-mimetic song repertories are learned from and shared with other males of the same species. We find that local dialect “neighborhoods” are variable in size among species and regions, depending on habitat continuity and the distribution of male territories. Despite the complete turnover of the specific songs comprising non-mimicry song repertoires from one local dialect to the next, we find significant species effects for more general measures of non-mimicry songs such as repertoire size and diversity, frequency, song length, and pace. For some traits, we also found significant regional differences, which may be mediated by significant relationships between elevation and morphometrics. Chatter calls were broadly similar across both species and localities, but we found significant species and region effects for frequency and to a lesser extent pace. We discuss the possibility that learning and mimicking the vocalizations of different hosts might influence the production of non-mimetic vocalizations and explain many of the species differences we detected. Whether these species differences are purely due to phenotypic plasticity or also reflect genetic divergence in traits influencing sound production and/or female preferences, they may contribute to reproductive isolation among nascent and recently evolved indigobird species.

Prolactin mediates behavioural rejection responses to avian brood parasitism

Adaptations resulting from co-evolutionary interactions between avian brood parasites and their hosts have been extensively studied, yet the physiological mechanisms underlying antiparasitic host defences remain little known. Prolactin, one of the main hormones involved in the regulation of avian parental behaviour, might play a key role in the orchestration of the host responses to avian brood parasitism. Given the positive association between prolactin and parental behaviour during incubation, decreasing prolactin levels are expected to facilitate egg-rejection decisions. We tested this prediction by implanting Eurasian blackbird (Turdus merula) females with an inhibitor of prolactin secretion, bromocriptine mesylate, to experimentally decrease their plasma prolactin levels. Bromocriptine-implanted individuals ejected mimetic model eggs at higher rates, and showed shorter latency to egg ejection, than placebo-treated birds. To our knowledge, this is the first experimental evidence that behavioural host defences against avian brood parasitism are mediated by prolactin.